Plumage brightness and uropygial gland secretions in barn swallows

Plumage brightness and uropygial gland secretions in barn swallows The uropygial gland has been hypothesized to play a role in sexual signaling through a “make-up” function derived from the effects of secretions from the gland on the appearance of the plumage and bare parts of the body. Here we show that plumage brightness of dorsal feathers of individual barn swallows Hirundo rustica was greater in mated than in unmated individuals. In addition, plumage brightness increased with colony size. Furthermore, plumage brightness was positively correlated with the amount of wax in the uropygial gland, negatively correlated with time of sam- pling of uropygial wax (perhaps because more wax is present early in the morning after an entire night of wax production without any preening), and negatively correlated with the number of chew- ing lice that degrade the plumage. Experimentally preventing barn swallows from access to the uropygial gland reduced plumage brightness, showing a causal link between secretions from the uropygial gland and plumage brightness. These findings provide evidence consistent with a role of uropygial secretions in signaling plumage brightness. Key words: brightness, coloration, preening wax, sexual selection, uropygial gland Many species of animals change their exterior phenotype by using attractiveness (e.g., Andersson and Amundsen 1996; Blanco et al. bodily or extra-bodily substances (reviews in Berthold 1967; 1999; Figuerola and Senar 2005; Galva ´ n and Sanz 2006). Lo ´ pez- Grammer et al. 2003; Montgomerie 2006; Delhey et al. 2007). Rull et al. (2010) and Pe ´ rez-Rodrı´guez et al. (2011) showed evi- The function of such use of substances for skin, plumage or pelage dence of a change in reflectance of plumage in response to applica- can broadly be divided into signaling or mating advantages and tion of wax. Several studies have suggested that soiling of the advantages in terms of antimicrobial defenses although these plumage may affect ultraviolet reflectance (Pe´rez-Rodrı´guez et al. explanations may not be mutually exclusive. The first hypothesis 2011; Surmacki 2011) by preventing or reducing reflectance from suggests that the use of substances that are applied to the body the surface of feathers that otherwise are covered by uropygial surface increases the attractiveness of an individual and thereby secretions. For example, Negro et al. (1999) suggested that the ap- improves its mating success or its success with respect to other plication of red ferro-oxide to the plumage of bearded vultures recipients of the visual signal. Several recent studies have sug- Gypaetus barbatus was due to its attractiveness, although a func- gested that secretions from the uropygial gland (an exocrine gland tional hypothesis suggesting an oxidative effect is just as compat- in birds that produces complex biochemicals that are smeared ible with available data (Arlettaz et al. 2002). Recently, Hirao with the beak across the plumage) may act as a cosmetic that et al. (2009) showed that cockerels Gallus domesticus copulated increases plumage brightness and hence improves sexual less frequently with uropygial glandectomized chickens than with V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 sham-operated females. They also showed that olfactory bulbec- We focused on the brightness of the dark color of the back, which tomized cocks copulated equally often with sham-operated and has been shown to be highly repeatable within years (Garamszegi uropygial glandectomized chickens, while sham-operated males et al. 2006). Surprisingly, plumage brightness has been the focus of copulated less often with uropygial glandectomized chickens than much less research than other components of coloration, which sham-operated females. These findings may reflect a role of the makes it a natural target of further study (Romano et al. 2017a, uropygial gland in sexual selection. 2010b). First, we tested the prediction that plumage brightness of The alternative functional hypothesis is that the application of male barn swallows is greater in mated than in unmated males. such external substances to skin or plumage is for antimicrobial use While there is an excess of males in the population, females always (Moreno-Rueda 2018). Secretions of the exocrine uropygial gland find a mate (Møller 1994). The blue dorsal plumage of male barn are complex, and interspecifically highly diverse chemical com- swallows is known to be 8–9% brighter than that of females, imply- pounds with known anti-microbial effects on bacteria and fungi (re- ing sexual dichromatism and hence a benefit in terms of sexual selec- view in Jacob and Ziswiler 1982). The extreme diversity of these tion (Perrier et al. 2002). Second, we tested if plumage brightness is biochemical compounds, as least compared to most other biochemi- related to degree of sociality as reflected by colony size. Barn swal- cals, and the fact that they have a strong phylogenetic signal, imply lows breeding in large colonies have more plumage-degrading bac- that they have been subject to intense selection, presumably caused teria than barn swallows from small colonies (Møller et al. 2009), by coevolutionary interactions between hosts and parasites. but it remains unknown whether colonial barn swallows produce Uropygial gland secretions have a negative effect on bacterial and more wax and hence have brighter plumage than solitarily breeding fungal infections of feathers and the skin (Jacob and Ziswiler 1982; conspecifics. We tested whether that was the case in the present Bandyopadhyay and Bhattacharyya 1996, 1999; Shawkey et al. study. Third, we tested if plumage brightness increases when an indi- 2003; Møller et al. 2009). Comparative studies have shown that vidual produces more wax. Fourth, we tested if plumage brightness there are significant viability effects associated with large uropygial depends on the time of collection of the feather sample. When a glands (Møller et al. 2010a, 2010b), and that large uropygial glands are associated with greater abundance of feather mites and a higher plumage sample was collected early in the morning, such a sample diversity of chewing lice in species of birds (Galva ´ n et al. 2008; would have been preened with larger amounts of wax that had accu- Møller et al. 2010a). Two publications by Galva ´ n et al. (2008; mulated during the night and deposited on feathers during the early Galva ´ n and Sanz 2006) related uropygial secretions to mite abun- morning peak in preening activity (Møller 1991b). This implies a dance. Pap et al. (2010), Mele ´ ndez et al. (2014), and Møller et al. direct effect of secretions from the uropygial gland on plumage (2010a, 2010b), however, did not find relationships between mite brightness. Fifth, we tested if barn swallows have brighter plumage abundance and uropygial gland size. Therefore, this relationship is when having few chewing lice that are known to degrade the plum- at best weak. Reneerkens et al. (2005) showed that many ground- age (Møller 1991a, 1994; Vas et al. 2008). Some previous studies nesting shorebirds and ducks (hence two independent evolutionary have also suggested that chewing lice may be affected by uropygial events) have evolved diester uropygial gland secretions that are less secretions (Møller et al. 2009; see also Moreno-Rueda 2010). volatile and potentially less easy to detect by predators than monest- Finally, we test if experimentally preventing access to the uropygial ers (at least for an olfactory-based searching dog). Furthermore, the gland reduced plumage brightness, as would be expected if secretions composition of these secretions changes over the annual cycle from from the uropygial gland were the cause of plumage brightness. monester during the non-breeding season to diester during the breeding season (Reneerkens et al. 2002, 2005). A function of secre- tions from the uropygial gland in predator deterrence (Steyn 1999) Materials and Methods or olfactory crypsis (Reneerkens et al. 2005) can be accommodated into an antimicrobial context. Some studies have shown that the size Uropygial glands and wax from glands of the uropygial gland is related to the expression of secondary sex- Barn swallows were captured at Kraghede, Denmark (57 12’N, ual characters (Galva ´ n and Sanz 2006; Moreno-Rueda 2010), while 10 00’E) during May–August 2008 and again in June 2012 in a other secondary sexual characters have shown no such relationship study population that has been followed since 1971 (Møller 1994). between the size of the gland and the expression of secondary sexual There were no survivors between 2008 and 2012 so there was no characters (Galva ´ n and Sanz 2006; Møller et al. 2009; Moreno- pseudo-replication. All barn swallows were provided by a numbered Rueda 2010). For nestling tawny owls Strix aluco that uropygial ring and color rings for individual identification and a number of gland secretions reduced rather than increased brightness of beak different measurements were taken, parasite abundance recorded color, and that production of wax from the uropygial gland is and blood samples extracted. impaired by a stimulation of the immune system (see also Moreno- APM measured the length, width and height of the uropygial gland Rueda 2015). Again, these results may suggest a role in crypsis ra- with a digital caliper with a precision of 0.01 mm. Subsequently vol- ther than make-up, and the effect of immune stimulation on produc- ume of the uropygial gland was calculated from these three linear tion of wax from the uropygial gland could reflect either a sexual measurements (Møller et al. 2009 for methods). This measure of exter- function with increased brightness being associated with uropygial nal gland size is strongly positively correlated with the mass of the gland secretions or an antimicrobial function with brighter color- gland when removed from the body in different species of birds ation being reflecting immunocompetence. (Møller et al. 2010a). The estimated size of the gland is highly repeat- The objectives of this article were to test the hypothesis that the able on different days (see Møller et al. 2009 for data). uropygial gland plays a role in plumage brightness. The barn Subsequently, APM extracted secretions from the uropygial gland swallow Hirundo rustica was used as a model system because indi- by gently touching it repeatedly with a 5 ll micro-capillary tube until viduals are easy to capture, follow and experimentally manipulate. secretions had ceased to emerge. The amount in the micro-capillary Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 Pape Møller and Mateos-Gonza ´ lez.  Plumage brightness and uropygial glands 3 tube was subsequently measured with a digital caliper to the nearest Table 1. Plumage brightness of adult barn swallows in relation to amount of uropygial wax, abundance of chewing lice and time dur- 0.001 ll. Seven barn swallows captured in the morning on two differ- ing the day when the wax sample was collected ent days showed a high degree of repeatability in amount of uropygial wax of 0.88 (SE ¼ 0.13) (based on ANOVA with individual identity Variable Sum of df F P Estimate Effect as classification variable, Møller et al. 2009). squares (SE) size Uropygial wax 17,208.28 1 8.41 0.0041 47.62 (16.42) 0.19 Colony size Time of sampling 33,413.84 1 16.32 <0.0001 0.041 (0.010) 0.26 Chewing lice 16,049.39 1 7.84 0.0056 16.803 (6.001) 0.19 We estimated colony size as the number of pairs breeding in a given site Tail length 11,370.55 1 5.55 0.019 0.945 (0.401) 0.16 throughout the breeding season because individuals hardly ever move Sex 13,622.72 1 6.65 0.011 12.024 (4.661) 0.17 from one breeding site to another once they have chosen a breeding site Error 446,297.73 218 (Møller 1994). Only 3 out of more than 4,000 individuals ever moved site and then always to the nearest neighboring site. The model had the statistics F ¼ 8.25, df ¼ 5, 218, r ¼ 0.14, P< 0.0001. Effect size was estimated as pearson’s product-moment correlation coefficient. Mating success and tail length different sampling days within a season, but also among seasons APM estimated mating success from the presence of a male and a fe- (Møller 1991a, 1994). In an experiment conducted in June 2015 at male within each of the small breeding territories at any time during Kraghede, Denmark, with a tail feather of a barn swallow placed in the breeding season (see Møller 1994 for details). Thus, males a petri dish in the dark at 38 C with 0, 5, or 25 chewing lice, there remained unmated throughout the entire breeding season as judged were no additional holes in feathers in the five dishes without chew- by their high singing activity and their continuous attempts to at- ing lice after 2 weeks, there was an increase by 1.4 holes (SE ¼ 0.51) tract females (Møller 1985). Only males were unmated. APM meas- in five dishes with five lice, and there was an increase by 5.4 holes ured the length of the tail to the nearest mm using a ruler with a (SE ¼ 0.75) in five dishes with 25 lice. These differences were sig- precision of 1 mm (see Møller 1994 for details). nificant in a GLM with a Poisson distribution and a log link func- tion (v ¼ 40.13, df ¼ 2, P< 0.0001). Plumage brightness APM collected a sample of 5–10 feathers from the centre of the blue Experimental manipulation of access to the back, the red throat, and the white belly of each individual barn swal- uropygial gland low before storing these feathers in zip-lock bags and in complete APM developed a small plastic container to place over the uropygial darkness until color measurements were made in October–December gland as previously done to prevent sperm transfer from the cloaca 2010. This should prevent fading, although the fact that all individuals (Michl et al. 2008). During early June 2012, the small 10 mm diam- were measured simultaneously should prevent any bias. FMG over- eter containers were either placed over the uropygial gland (treat- lapped five blue back feathers from each sample, simulating their nat- ment) or just above the uropygial gland (controls) of males using a ural position on the bird, on a receptacle made from black matte string attached with glue to the container. APM captured 26 birds cardboard. Spectral reflectance data, relative to a white reflectance and assigned these randomly to the treatment or the control group. standard, were obtained from these samples (N ¼ 228) using an The birds were recaptured 10 days later, and all but one still had the Avantes AvaSpec-2048 spectrometer provided with a deuterium- small container attached to the body, as at the start of the experi- halogen light source (Avantes, Eerbek, Netherlands). ment, showing that the treatment was effective. The single individ- The end of the reflectance probe was fitted with a black plastic ual without a container was eliminated from the analyses. Feathers cylinder that helped to block the ambient light and to keep a stand- were removed from the back at recapture as described above and ardized distance to the feathers (approximately 2 mm). Three repli- plumage brightness was subsequently measured. cate readings were taken from each sample, holding the probe at 90 . The spectrometer was recalibrated after measuring each indi- vidual. Data on plumage brightness were computed using Avasoft Statistical analyses 7.1, obtaining reflectance values from 300 to 700 nm, averaged We log -transformed the abundance of parasites (by adding a con- every 10 nm. Brightness was calculated as the total amount of light stant of one), gland size, volume of secretions from the uropygial reflected by the feathers, by summing up the total reflectance gland, and colony size. Brightness fulfilled the criterion for homosce- obtained along the wavelength range 300–700 nm (Endler 1990). dasticity (Shapiron–Wilk W-test, W< 0.98, P> 0.13). FMG made all color measurements blindly with respect to informa- We compared plumage brightness, parasite abundance, gland tion on uropygial wax or other variables, preventing any bias in size, and amount of secretions between sexes and between mated measurements. Repeatability of brightness for a small sample of and unmated individuals, respectively, using JMP version 10 (SAS nine individuals sampled twice was F ¼ 86.77, df ¼ 8, 9, r ¼ 0.98, 2012). Only males were unmated so mating status and sex could not P< 0.0001, R ¼ 0.98 (SE ¼ 0.02)). be included in the same model. Likewise, we related these variables to colony size by using mean values per colony. Chewing lice and feather mites We developed best-fit generalized linear models by reducing full Upon capture APM counted the number of holes in the feathers of models (including the volume of uropygial secretions, body mass, wings and tail of adult barn swallows, which were presumably made time of sampling, the number of chewing lice, the number of feather by the chewing louse Brueelia sp. (Møller 1991a; Vas et al. 2008), mites, tail length, and tarsus length) until the final model only con- although other causes (e.g., feather-degrading bacteria, see Fu ¨lo ¨p tained factors with an associated P< 0.10. These models are reported et al. 2016) have been proposed (review in Va ´ga ´ si 2014). These in the ‘Results’ section or in Table 1. To assess possible problems of holes are clearly visible when the feathers are held against a light collinearity, we calculated variance inflation factors that in all cases source. The abundance of holes is highly repeatable not only on were less than 3, which is much less than the commonly accepted Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Plumage brightness, amount of wax in uropygial glands and parasites Plumage brightness was predicted by five factors that explained 14% of the variance (Table 1). Brightness increased with the amount of uropygial wax, with an intermediate effect size (Figure 2A). When plumage was sampled earlier in the morning, plumage bright- ness was greater, with an intermediate effect size (Figure 2B). Plumage brightness increased with tail length (Table 1). Plumage brightness was higher in males than in females (Table 1). Finally, barn swallows with more chewing lice had less bright plumage col- oration, with an intermediate effect size (Figure 2C). In contrast, there was no significant effect of feather mites on plumage bright- ness (F ¼ 0.23, df ¼ 1, 225, P ¼ 0.63). 1 10 100 Experimental manipulation of uropygial glands and Colony size (pairs) plumage brightness Figure 1. Mean plumage brightness of dorsal feathers for barn swallows in Experimental birds had significantly more wax in their uropygial relation to colony size. 2 glands than controls (F ¼ 8.66, df ¼ 1, 23, r ¼ 0.27, P ¼ 0.0073; ex- perimental: 2.05 (0.03), control: 1.84 (0.07)). Plumage brightness was lower in the group of experimental birds compared to the con- levels for significant collinearity of 5–10 (McClave and Sincich 2003). trols (Figure 3; F ¼ 8.40, df ¼ 1, 23, r ¼ 0.27, P ¼ 0.0079). We tested for effects of the experiment on amount of secretion and plumage brightness using experimental treatment as a factor. Effect size was estimated as Pearson’s product–moment correlation coefficient is a standardized measure of the magnitude of effects Discussion r (Rosenthal 1994). We assessed relationships based on effect sizes To summarize, plumage brightness of adult barn swallows differed according to the criteria listed by Cohen (1988) for small (Pearson significantly between mated and unmated individuals and increased r ¼ 0.10, explaining 1% of the variance), intermediate (Pearson with colony size. Brightness was greater in individuals that had r ¼ 0.30; 9% of the variance), or large effects (Pearson r ¼ 0.50; 25% more uropygial wax, when feathers were sampled earlier in the of the variance). All values reported are means (SE). morning and when there were few chewing lice. Experimentally pre- venting birds from access to the uropygial gland caused a decrease in plumage brightness. This finding is consistent with another study Results showing that changes in uropygial gland size are correlated with Plumage brightness, mating status, and colony size changes in bib coloration in house sparrows Passer domesticus We recorded plumage brightness of the blue feathers from the back (Moreno-Rueda 2016). These findings match with key predictions of adult male and female barn swallows. Plumage brightness was on of the make-up hypothesis, that is, that uropygial wax or other sub- average 157 (SE ¼ 3), range 59–303, N ¼ 228. A total of 114 mated stances should enhance the brightness of plumage or naked body male barn swallows had brighter plumage than the five unmated parts (Andersson and Amundsen 1996; Blanco et al. 1999; Piersma swallows (F ¼ 10.75, df ¼ 1, P ¼ 0.001). Plumage brightness for et al. 1999; Figuerola and Senar 2005; Galva ´ n and Sanz 2006; mated males was 155 (5), N ¼ 114, compared to 94 (18), N ¼ 6 Montgomerie 2006; Delhey et al. 2007), with this increased bright- unmated males. This effect of plumage brightness was independent ness providing a mating advantage. of tail length (partial effect of brightness on mating success after in- West-Eberhard (1983) has suggested that many characters have clusion of tail length as an additional predictor of mating success evolved as a means of facilitating social competition. Plumage (F ¼ 4.36, df ¼ 1, P ¼ 0.008). Brightness was significantly larger in brightness increased strongly and significantly with degree of social- males than in females (F ¼ 8.24, df ¼ 1, 224, P ¼ 0.0045; males: ity as reflected by colony size in the barn swallow. This correlation 143 (6), females: 172 (6)), and increased with tail length (F ¼ 7.20, may arise as a consequence of (1) differential recruitment of individ- df ¼ 1, 224, P ¼ 0.0078, slope (SE) ¼ 1.14 (0.43)]. uals with particularly bright plumage to large colonies, (2) larger Mean plumage brightness of males and females combined uropygial glands and hence more secretions in birds from larger col- increased with colony size [Figure 1; linear regression based on onies, or (3) a difference in abundance of microorganisms among mean brightness for ten colonies: F ¼ 32.01, df ¼ 1, 8, r ¼ 0.80, barn swallows breeding in colonies of different sizes. Møller et al. P ¼ 0.0005, slope (ES) ¼ 21.22 (3.75)]. Thus, plumage brightness (2009) have previously reported that barn swallows breeding in was greater in larger colonies. large colonies have significantly more feather degrading bacteria The amount of uropygial wax was slightly larger in females than in than conspecifics breeding solitarily or in small colonies. We found males [F¼ 4.57, df ¼ 1, 223, r ¼ 0.02, P ¼ 0.03; males: 1.96 (0.02), a significant increase in the amount of secretions and size of uro- females: 2.01 (0.02)], while there was no significant difference in gland pygial glands among barn swallows from colonies of different sizes size between males and females (F¼ 0.68, df ¼ 1, 223, r ¼ 0.003, (Møller et al. 2009). We were unable to discriminate among these P¼ 0.41). The amount of uropygial wax was not related to colony size hypotheses with available data. (F¼ 0.10, df ¼ 1, 223, r ¼ 0.0005, P¼ 0.75), nor was the abundance We found evidence consistent with microbes and ectoparasites of chewing lice (F¼ 2.47, df ¼ 1, 223, r ¼ 0.01, P ¼ 0.12). The rela- affecting plumage brightness. Barn swallows with small uropygial tionship beween the size of the uropygial gland and colony size was not glands have previously been shown to have more feather degrading significant either (F¼ 1.05, df ¼ 1, 223, r ¼ 0.0005, P ¼ 0.31). bacteria (Møller et al. 2009) and hence less bright plumage than Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 Plumage brightness Pape Møller and Mateos-Gonza ´ lez.  Plumage brightness and uropygial glands 5 Figure 2. Plumage brightness of dorsal feathers for individual barn swallows in relation to (A) amount of uropygial wax (ll), (B) time of day [ranging from 0 (0) to 24 (2400)] when wax was sampled, and (C) number of chewing lice in adult barn swallows. The lines are the regression lines. In conclusion, the plumage of barn swallows was brighter in mated than in unmated individuals, in accordance to the hypothesis that plumage brightness is a sexually selected trait. Individuals with brighter plumage bred in larger colonies showing an associ- ation between plumage brightness and sociality. Plumage brightness increased with the amount of uropygial wax and the time when feathers were sampled, and with a decrease in the abundance of chewing lice that damage feathers through feeding. An experimental reduction in access to uropygial wax reduced plumage brightness providing direct evidence for a causal link between plumage bright- ness and uropygial wax. 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J Parasitol 94:1438–1440. body condition and wingbar size in the house sparrow Passer domesticus. West-Eberhard MJ, 1983. Sexual selection, social competition, and speciation. J Avian Biol 41:229–236. Q Rev Biol 58:155–183. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Plumage brightness and uropygial gland secretions in barn swallows

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Abstract

The uropygial gland has been hypothesized to play a role in sexual signaling through a “make-up” function derived from the effects of secretions from the gland on the appearance of the plumage and bare parts of the body. Here we show that plumage brightness of dorsal feathers of individual barn swallows Hirundo rustica was greater in mated than in unmated individuals. In addition, plumage brightness increased with colony size. Furthermore, plumage brightness was positively correlated with the amount of wax in the uropygial gland, negatively correlated with time of sam- pling of uropygial wax (perhaps because more wax is present early in the morning after an entire night of wax production without any preening), and negatively correlated with the number of chew- ing lice that degrade the plumage. Experimentally preventing barn swallows from access to the uropygial gland reduced plumage brightness, showing a causal link between secretions from the uropygial gland and plumage brightness. These findings provide evidence consistent with a role of uropygial secretions in signaling plumage brightness. Key words: brightness, coloration, preening wax, sexual selection, uropygial gland Many species of animals change their exterior phenotype by using attractiveness (e.g., Andersson and Amundsen 1996; Blanco et al. bodily or extra-bodily substances (reviews in Berthold 1967; 1999; Figuerola and Senar 2005; Galva ´ n and Sanz 2006). Lo ´ pez- Grammer et al. 2003; Montgomerie 2006; Delhey et al. 2007). Rull et al. (2010) and Pe ´ rez-Rodrı´guez et al. (2011) showed evi- The function of such use of substances for skin, plumage or pelage dence of a change in reflectance of plumage in response to applica- can broadly be divided into signaling or mating advantages and tion of wax. Several studies have suggested that soiling of the advantages in terms of antimicrobial defenses although these plumage may affect ultraviolet reflectance (Pe´rez-Rodrı´guez et al. explanations may not be mutually exclusive. The first hypothesis 2011; Surmacki 2011) by preventing or reducing reflectance from suggests that the use of substances that are applied to the body the surface of feathers that otherwise are covered by uropygial surface increases the attractiveness of an individual and thereby secretions. For example, Negro et al. (1999) suggested that the ap- improves its mating success or its success with respect to other plication of red ferro-oxide to the plumage of bearded vultures recipients of the visual signal. Several recent studies have sug- Gypaetus barbatus was due to its attractiveness, although a func- gested that secretions from the uropygial gland (an exocrine gland tional hypothesis suggesting an oxidative effect is just as compat- in birds that produces complex biochemicals that are smeared ible with available data (Arlettaz et al. 2002). Recently, Hirao with the beak across the plumage) may act as a cosmetic that et al. (2009) showed that cockerels Gallus domesticus copulated increases plumage brightness and hence improves sexual less frequently with uropygial glandectomized chickens than with V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 sham-operated females. They also showed that olfactory bulbec- We focused on the brightness of the dark color of the back, which tomized cocks copulated equally often with sham-operated and has been shown to be highly repeatable within years (Garamszegi uropygial glandectomized chickens, while sham-operated males et al. 2006). Surprisingly, plumage brightness has been the focus of copulated less often with uropygial glandectomized chickens than much less research than other components of coloration, which sham-operated females. These findings may reflect a role of the makes it a natural target of further study (Romano et al. 2017a, uropygial gland in sexual selection. 2010b). First, we tested the prediction that plumage brightness of The alternative functional hypothesis is that the application of male barn swallows is greater in mated than in unmated males. such external substances to skin or plumage is for antimicrobial use While there is an excess of males in the population, females always (Moreno-Rueda 2018). Secretions of the exocrine uropygial gland find a mate (Møller 1994). The blue dorsal plumage of male barn are complex, and interspecifically highly diverse chemical com- swallows is known to be 8–9% brighter than that of females, imply- pounds with known anti-microbial effects on bacteria and fungi (re- ing sexual dichromatism and hence a benefit in terms of sexual selec- view in Jacob and Ziswiler 1982). The extreme diversity of these tion (Perrier et al. 2002). Second, we tested if plumage brightness is biochemical compounds, as least compared to most other biochemi- related to degree of sociality as reflected by colony size. Barn swal- cals, and the fact that they have a strong phylogenetic signal, imply lows breeding in large colonies have more plumage-degrading bac- that they have been subject to intense selection, presumably caused teria than barn swallows from small colonies (Møller et al. 2009), by coevolutionary interactions between hosts and parasites. but it remains unknown whether colonial barn swallows produce Uropygial gland secretions have a negative effect on bacterial and more wax and hence have brighter plumage than solitarily breeding fungal infections of feathers and the skin (Jacob and Ziswiler 1982; conspecifics. We tested whether that was the case in the present Bandyopadhyay and Bhattacharyya 1996, 1999; Shawkey et al. study. Third, we tested if plumage brightness increases when an indi- 2003; Møller et al. 2009). Comparative studies have shown that vidual produces more wax. Fourth, we tested if plumage brightness there are significant viability effects associated with large uropygial depends on the time of collection of the feather sample. When a glands (Møller et al. 2010a, 2010b), and that large uropygial glands are associated with greater abundance of feather mites and a higher plumage sample was collected early in the morning, such a sample diversity of chewing lice in species of birds (Galva ´ n et al. 2008; would have been preened with larger amounts of wax that had accu- Møller et al. 2010a). Two publications by Galva ´ n et al. (2008; mulated during the night and deposited on feathers during the early Galva ´ n and Sanz 2006) related uropygial secretions to mite abun- morning peak in preening activity (Møller 1991b). This implies a dance. Pap et al. (2010), Mele ´ ndez et al. (2014), and Møller et al. direct effect of secretions from the uropygial gland on plumage (2010a, 2010b), however, did not find relationships between mite brightness. Fifth, we tested if barn swallows have brighter plumage abundance and uropygial gland size. Therefore, this relationship is when having few chewing lice that are known to degrade the plum- at best weak. Reneerkens et al. (2005) showed that many ground- age (Møller 1991a, 1994; Vas et al. 2008). Some previous studies nesting shorebirds and ducks (hence two independent evolutionary have also suggested that chewing lice may be affected by uropygial events) have evolved diester uropygial gland secretions that are less secretions (Møller et al. 2009; see also Moreno-Rueda 2010). volatile and potentially less easy to detect by predators than monest- Finally, we test if experimentally preventing access to the uropygial ers (at least for an olfactory-based searching dog). Furthermore, the gland reduced plumage brightness, as would be expected if secretions composition of these secretions changes over the annual cycle from from the uropygial gland were the cause of plumage brightness. monester during the non-breeding season to diester during the breeding season (Reneerkens et al. 2002, 2005). A function of secre- tions from the uropygial gland in predator deterrence (Steyn 1999) Materials and Methods or olfactory crypsis (Reneerkens et al. 2005) can be accommodated into an antimicrobial context. Some studies have shown that the size Uropygial glands and wax from glands of the uropygial gland is related to the expression of secondary sex- Barn swallows were captured at Kraghede, Denmark (57 12’N, ual characters (Galva ´ n and Sanz 2006; Moreno-Rueda 2010), while 10 00’E) during May–August 2008 and again in June 2012 in a other secondary sexual characters have shown no such relationship study population that has been followed since 1971 (Møller 1994). between the size of the gland and the expression of secondary sexual There were no survivors between 2008 and 2012 so there was no characters (Galva ´ n and Sanz 2006; Møller et al. 2009; Moreno- pseudo-replication. All barn swallows were provided by a numbered Rueda 2010). For nestling tawny owls Strix aluco that uropygial ring and color rings for individual identification and a number of gland secretions reduced rather than increased brightness of beak different measurements were taken, parasite abundance recorded color, and that production of wax from the uropygial gland is and blood samples extracted. impaired by a stimulation of the immune system (see also Moreno- APM measured the length, width and height of the uropygial gland Rueda 2015). Again, these results may suggest a role in crypsis ra- with a digital caliper with a precision of 0.01 mm. Subsequently vol- ther than make-up, and the effect of immune stimulation on produc- ume of the uropygial gland was calculated from these three linear tion of wax from the uropygial gland could reflect either a sexual measurements (Møller et al. 2009 for methods). This measure of exter- function with increased brightness being associated with uropygial nal gland size is strongly positively correlated with the mass of the gland secretions or an antimicrobial function with brighter color- gland when removed from the body in different species of birds ation being reflecting immunocompetence. (Møller et al. 2010a). The estimated size of the gland is highly repeat- The objectives of this article were to test the hypothesis that the able on different days (see Møller et al. 2009 for data). uropygial gland plays a role in plumage brightness. The barn Subsequently, APM extracted secretions from the uropygial gland swallow Hirundo rustica was used as a model system because indi- by gently touching it repeatedly with a 5 ll micro-capillary tube until viduals are easy to capture, follow and experimentally manipulate. secretions had ceased to emerge. The amount in the micro-capillary Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 Pape Møller and Mateos-Gonza ´ lez.  Plumage brightness and uropygial glands 3 tube was subsequently measured with a digital caliper to the nearest Table 1. Plumage brightness of adult barn swallows in relation to amount of uropygial wax, abundance of chewing lice and time dur- 0.001 ll. Seven barn swallows captured in the morning on two differ- ing the day when the wax sample was collected ent days showed a high degree of repeatability in amount of uropygial wax of 0.88 (SE ¼ 0.13) (based on ANOVA with individual identity Variable Sum of df F P Estimate Effect as classification variable, Møller et al. 2009). squares (SE) size Uropygial wax 17,208.28 1 8.41 0.0041 47.62 (16.42) 0.19 Colony size Time of sampling 33,413.84 1 16.32 <0.0001 0.041 (0.010) 0.26 Chewing lice 16,049.39 1 7.84 0.0056 16.803 (6.001) 0.19 We estimated colony size as the number of pairs breeding in a given site Tail length 11,370.55 1 5.55 0.019 0.945 (0.401) 0.16 throughout the breeding season because individuals hardly ever move Sex 13,622.72 1 6.65 0.011 12.024 (4.661) 0.17 from one breeding site to another once they have chosen a breeding site Error 446,297.73 218 (Møller 1994). Only 3 out of more than 4,000 individuals ever moved site and then always to the nearest neighboring site. The model had the statistics F ¼ 8.25, df ¼ 5, 218, r ¼ 0.14, P< 0.0001. Effect size was estimated as pearson’s product-moment correlation coefficient. Mating success and tail length different sampling days within a season, but also among seasons APM estimated mating success from the presence of a male and a fe- (Møller 1991a, 1994). In an experiment conducted in June 2015 at male within each of the small breeding territories at any time during Kraghede, Denmark, with a tail feather of a barn swallow placed in the breeding season (see Møller 1994 for details). Thus, males a petri dish in the dark at 38 C with 0, 5, or 25 chewing lice, there remained unmated throughout the entire breeding season as judged were no additional holes in feathers in the five dishes without chew- by their high singing activity and their continuous attempts to at- ing lice after 2 weeks, there was an increase by 1.4 holes (SE ¼ 0.51) tract females (Møller 1985). Only males were unmated. APM meas- in five dishes with five lice, and there was an increase by 5.4 holes ured the length of the tail to the nearest mm using a ruler with a (SE ¼ 0.75) in five dishes with 25 lice. These differences were sig- precision of 1 mm (see Møller 1994 for details). nificant in a GLM with a Poisson distribution and a log link func- tion (v ¼ 40.13, df ¼ 2, P< 0.0001). Plumage brightness APM collected a sample of 5–10 feathers from the centre of the blue Experimental manipulation of access to the back, the red throat, and the white belly of each individual barn swal- uropygial gland low before storing these feathers in zip-lock bags and in complete APM developed a small plastic container to place over the uropygial darkness until color measurements were made in October–December gland as previously done to prevent sperm transfer from the cloaca 2010. This should prevent fading, although the fact that all individuals (Michl et al. 2008). During early June 2012, the small 10 mm diam- were measured simultaneously should prevent any bias. FMG over- eter containers were either placed over the uropygial gland (treat- lapped five blue back feathers from each sample, simulating their nat- ment) or just above the uropygial gland (controls) of males using a ural position on the bird, on a receptacle made from black matte string attached with glue to the container. APM captured 26 birds cardboard. Spectral reflectance data, relative to a white reflectance and assigned these randomly to the treatment or the control group. standard, were obtained from these samples (N ¼ 228) using an The birds were recaptured 10 days later, and all but one still had the Avantes AvaSpec-2048 spectrometer provided with a deuterium- small container attached to the body, as at the start of the experi- halogen light source (Avantes, Eerbek, Netherlands). ment, showing that the treatment was effective. The single individ- The end of the reflectance probe was fitted with a black plastic ual without a container was eliminated from the analyses. Feathers cylinder that helped to block the ambient light and to keep a stand- were removed from the back at recapture as described above and ardized distance to the feathers (approximately 2 mm). Three repli- plumage brightness was subsequently measured. cate readings were taken from each sample, holding the probe at 90 . The spectrometer was recalibrated after measuring each indi- vidual. Data on plumage brightness were computed using Avasoft Statistical analyses 7.1, obtaining reflectance values from 300 to 700 nm, averaged We log -transformed the abundance of parasites (by adding a con- every 10 nm. Brightness was calculated as the total amount of light stant of one), gland size, volume of secretions from the uropygial reflected by the feathers, by summing up the total reflectance gland, and colony size. Brightness fulfilled the criterion for homosce- obtained along the wavelength range 300–700 nm (Endler 1990). dasticity (Shapiron–Wilk W-test, W< 0.98, P> 0.13). FMG made all color measurements blindly with respect to informa- We compared plumage brightness, parasite abundance, gland tion on uropygial wax or other variables, preventing any bias in size, and amount of secretions between sexes and between mated measurements. Repeatability of brightness for a small sample of and unmated individuals, respectively, using JMP version 10 (SAS nine individuals sampled twice was F ¼ 86.77, df ¼ 8, 9, r ¼ 0.98, 2012). Only males were unmated so mating status and sex could not P< 0.0001, R ¼ 0.98 (SE ¼ 0.02)). be included in the same model. Likewise, we related these variables to colony size by using mean values per colony. Chewing lice and feather mites We developed best-fit generalized linear models by reducing full Upon capture APM counted the number of holes in the feathers of models (including the volume of uropygial secretions, body mass, wings and tail of adult barn swallows, which were presumably made time of sampling, the number of chewing lice, the number of feather by the chewing louse Brueelia sp. (Møller 1991a; Vas et al. 2008), mites, tail length, and tarsus length) until the final model only con- although other causes (e.g., feather-degrading bacteria, see Fu ¨lo ¨p tained factors with an associated P< 0.10. These models are reported et al. 2016) have been proposed (review in Va ´ga ´ si 2014). These in the ‘Results’ section or in Table 1. To assess possible problems of holes are clearly visible when the feathers are held against a light collinearity, we calculated variance inflation factors that in all cases source. The abundance of holes is highly repeatable not only on were less than 3, which is much less than the commonly accepted Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Plumage brightness, amount of wax in uropygial glands and parasites Plumage brightness was predicted by five factors that explained 14% of the variance (Table 1). Brightness increased with the amount of uropygial wax, with an intermediate effect size (Figure 2A). When plumage was sampled earlier in the morning, plumage bright- ness was greater, with an intermediate effect size (Figure 2B). Plumage brightness increased with tail length (Table 1). Plumage brightness was higher in males than in females (Table 1). Finally, barn swallows with more chewing lice had less bright plumage col- oration, with an intermediate effect size (Figure 2C). In contrast, there was no significant effect of feather mites on plumage bright- ness (F ¼ 0.23, df ¼ 1, 225, P ¼ 0.63). 1 10 100 Experimental manipulation of uropygial glands and Colony size (pairs) plumage brightness Figure 1. Mean plumage brightness of dorsal feathers for barn swallows in Experimental birds had significantly more wax in their uropygial relation to colony size. 2 glands than controls (F ¼ 8.66, df ¼ 1, 23, r ¼ 0.27, P ¼ 0.0073; ex- perimental: 2.05 (0.03), control: 1.84 (0.07)). Plumage brightness was lower in the group of experimental birds compared to the con- levels for significant collinearity of 5–10 (McClave and Sincich 2003). trols (Figure 3; F ¼ 8.40, df ¼ 1, 23, r ¼ 0.27, P ¼ 0.0079). We tested for effects of the experiment on amount of secretion and plumage brightness using experimental treatment as a factor. Effect size was estimated as Pearson’s product–moment correlation coefficient is a standardized measure of the magnitude of effects Discussion r (Rosenthal 1994). We assessed relationships based on effect sizes To summarize, plumage brightness of adult barn swallows differed according to the criteria listed by Cohen (1988) for small (Pearson significantly between mated and unmated individuals and increased r ¼ 0.10, explaining 1% of the variance), intermediate (Pearson with colony size. Brightness was greater in individuals that had r ¼ 0.30; 9% of the variance), or large effects (Pearson r ¼ 0.50; 25% more uropygial wax, when feathers were sampled earlier in the of the variance). All values reported are means (SE). morning and when there were few chewing lice. Experimentally pre- venting birds from access to the uropygial gland caused a decrease in plumage brightness. This finding is consistent with another study Results showing that changes in uropygial gland size are correlated with Plumage brightness, mating status, and colony size changes in bib coloration in house sparrows Passer domesticus We recorded plumage brightness of the blue feathers from the back (Moreno-Rueda 2016). These findings match with key predictions of adult male and female barn swallows. Plumage brightness was on of the make-up hypothesis, that is, that uropygial wax or other sub- average 157 (SE ¼ 3), range 59–303, N ¼ 228. A total of 114 mated stances should enhance the brightness of plumage or naked body male barn swallows had brighter plumage than the five unmated parts (Andersson and Amundsen 1996; Blanco et al. 1999; Piersma swallows (F ¼ 10.75, df ¼ 1, P ¼ 0.001). Plumage brightness for et al. 1999; Figuerola and Senar 2005; Galva ´ n and Sanz 2006; mated males was 155 (5), N ¼ 114, compared to 94 (18), N ¼ 6 Montgomerie 2006; Delhey et al. 2007), with this increased bright- unmated males. This effect of plumage brightness was independent ness providing a mating advantage. of tail length (partial effect of brightness on mating success after in- West-Eberhard (1983) has suggested that many characters have clusion of tail length as an additional predictor of mating success evolved as a means of facilitating social competition. Plumage (F ¼ 4.36, df ¼ 1, P ¼ 0.008). Brightness was significantly larger in brightness increased strongly and significantly with degree of social- males than in females (F ¼ 8.24, df ¼ 1, 224, P ¼ 0.0045; males: ity as reflected by colony size in the barn swallow. This correlation 143 (6), females: 172 (6)), and increased with tail length (F ¼ 7.20, may arise as a consequence of (1) differential recruitment of individ- df ¼ 1, 224, P ¼ 0.0078, slope (SE) ¼ 1.14 (0.43)]. uals with particularly bright plumage to large colonies, (2) larger Mean plumage brightness of males and females combined uropygial glands and hence more secretions in birds from larger col- increased with colony size [Figure 1; linear regression based on onies, or (3) a difference in abundance of microorganisms among mean brightness for ten colonies: F ¼ 32.01, df ¼ 1, 8, r ¼ 0.80, barn swallows breeding in colonies of different sizes. Møller et al. P ¼ 0.0005, slope (ES) ¼ 21.22 (3.75)]. Thus, plumage brightness (2009) have previously reported that barn swallows breeding in was greater in larger colonies. large colonies have significantly more feather degrading bacteria The amount of uropygial wax was slightly larger in females than in than conspecifics breeding solitarily or in small colonies. We found males [F¼ 4.57, df ¼ 1, 223, r ¼ 0.02, P ¼ 0.03; males: 1.96 (0.02), a significant increase in the amount of secretions and size of uro- females: 2.01 (0.02)], while there was no significant difference in gland pygial glands among barn swallows from colonies of different sizes size between males and females (F¼ 0.68, df ¼ 1, 223, r ¼ 0.003, (Møller et al. 2009). We were unable to discriminate among these P¼ 0.41). The amount of uropygial wax was not related to colony size hypotheses with available data. (F¼ 0.10, df ¼ 1, 223, r ¼ 0.0005, P¼ 0.75), nor was the abundance We found evidence consistent with microbes and ectoparasites of chewing lice (F¼ 2.47, df ¼ 1, 223, r ¼ 0.01, P ¼ 0.12). The rela- affecting plumage brightness. Barn swallows with small uropygial tionship beween the size of the uropygial gland and colony size was not glands have previously been shown to have more feather degrading significant either (F¼ 1.05, df ¼ 1, 223, r ¼ 0.0005, P ¼ 0.31). bacteria (Møller et al. 2009) and hence less bright plumage than Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy042/5025951 by guest on 13 July 2018 Plumage brightness Pape Møller and Mateos-Gonza ´ lez.  Plumage brightness and uropygial glands 5 Figure 2. Plumage brightness of dorsal feathers for individual barn swallows in relation to (A) amount of uropygial wax (ll), (B) time of day [ranging from 0 (0) to 24 (2400)] when wax was sampled, and (C) number of chewing lice in adult barn swallows. The lines are the regression lines. In conclusion, the plumage of barn swallows was brighter in mated than in unmated individuals, in accordance to the hypothesis that plumage brightness is a sexually selected trait. Individuals with brighter plumage bred in larger colonies showing an associ- ation between plumage brightness and sociality. Plumage brightness increased with the amount of uropygial wax and the time when feathers were sampled, and with a decrease in the abundance of chewing lice that damage feathers through feeding. An experimental reduction in access to uropygial wax reduced plumage brightness providing direct evidence for a causal link between plumage bright- ness and uropygial wax. 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